Reductive evolution and unique infection and feeding mode in the CPR predatory bacterium Vampirococcus lugosii

Abstract

The Candidate Phyla Radiation (CPR) constitutes a large supergroup of mostly uncultured bacterial lineages discovered through metabarcoding and metagenomics in diverse environments. Having small cell sizes, reduced genomes, and limited biosynthetic capabilities, they are thought to be symbionts of other organisms from which they obtain essential biomolecules. However, the nature of this symbiosis (mutualistic, neutral, or parasitic) has been ascertained only for rare cultured members of the CPR phylum Saccharibacteria, which are epibiotic parasites of other bacteria. Here, we characterize the biology and the genome of Vampirococcus lugosii, which becomes the first described species of Vampirococcus, a genus of epibiotic bacteria morphologically identified decades ago. Vampirococcus belongs to the CPR phylum Absconditabacteria. It feeds on anoxygenic photosynthetic gammaproteobacteria, fully absorbing their cytoplasmic content. The cells divide epibiotically, forming multicellular stalks whose apical cells can more easily reach new hosts. Vampirococcus genome is small (1.3 Mbp) and highly reduced in biosynthetic metabolism genes. However, it is enriched in genes related to an elaborate, fibrous cell surface likely involved in complex interactions with the host. Comparative genomic analyses show that gene loss has been continuous during Absconditabacteria, and generally most CPR bacteria, evolution. Nonetheless, gene loss was compensated by gene acquisition by horizontal gene transfer and evolution de novo. In Vampirococcus, these innovations include new CRISPR-Cas effectors and a novel electron transport chain. Our findings confirm parasitism as a widespread lifestyle of CPR bacteria, which probably play a previously neglected virus-like ecological role in ecosystems, controlling bacterial populations by a unique form of predation.